'Life-style' control networks in Escherichia coli: Signaling by the second messenger c-di-GMP

Journal of Biotechnology

Volumn 160, Issue 1-2, 2012, Pages 10-16

  Povolotsky, Tatyana L ^a   Hengge, Regine ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Biofilm; Cyclic di GMP; EAL domain; GGDEF domain; Motility; RpoS

Indexed keywords

CYCLIC-DI-GMP; EAL DOMAIN; GGDEF DOMAIN; MOTILITY; RPOS;

BACTERIA; BIOFILMS; ESCHERICHIA COLI; GENE EXPRESSION; GYPSUM; PROTEINS; SIGNALING;

MOLECULAR BIOLOGY;

ADHESIN; AMINO ACID; BACTERIAL PROTEIN; CYCLIC DIGUANYLATE; CYCLIC GMP DERIVATIVE; PHOSPHODIESTERASE; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BINDING SITE; CAULOBACTER CRESCENTUS; CELL MOTILITY; CHROMATOPHORE; DOWN REGULATION; ESCHERICHIA COLI; FIMBRIA; GENE EXPRESSION; GLUCONACETOBACTER XYLINUS; HYDROLYSIS; INTRON; MICROBIAL DIVERSITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE; XANTHOMONAS;

BIOFILMS; CYCLIC GMP; ESCHERICHIA COLI; SECOND MESSENGER SYSTEMS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84862225191     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2011.12.024     Document Type: Article

References (85)

1. Amikam D., Galperin M.Y. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 2006, 22:3-6.
2. Anderson K.L., Whitlock J.E., Harwood V.J. Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments. Appl. Environ. Microbiol. 2005, 71:3041-3048.
3. Andrade M.O., Alegria M.C., Guzzo C.R., Docena C., Rosa M.C., Ramos C.H., Farah C.S. The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv. citri. Mol. Microbiol. 2006, 62:537-551.
4. Babitzke P., Romeo T. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol. 2007, 10:156-163.
5. Barends T.R., Hartmann E., Griese J.J., Beitlich T., Kirienko N.V., Ryjenkov D.A., Reinstein J., Shoeman R.L., Gomelsky M.I.S. Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 2009, 18:1015-1018.
6. Barnhart M.M., Chapman M.R. Curli biogenesis and function. Annu. Rev. Microbiol. 2006, 60:131-147.
7. Bielaszewska M., Mellmann A., Zhang W., Köck R., Fruth A., Bauwens A., Peters G., Karch H. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect. Dis. 2011, 11:671-676.
8. Bobrov A.G., Kirillina O., Forman S., Mack D., Perry R.D. Insights into Yersinia pestis biofilm development: topology and co-interaction of Hms inner membrane proteins involved in exopolysaccharide production. Environ. Microbiol. 2008, 10:1419-1432.
9. Boehm A., Steiner S., Zaehringer F., Casanova A., Hamburger F., Ritz D., Keck W., Ackerman M., Schirmer T., Jenal U. Second messenger signaling governs Escherichia coli biofilm induction upon ribosomal stress. Mol. Microbiol. 2009, 72:1500-1516.
10. Boehm A., Kaiser M., Li H., Spangler C., Kasper C.A., Ackerman M., Kaever V., Sourjik V., Roth V., Jenal U. Second messenger-mediated adjustment of bacterial swimming velocity. Cell 2010, 141:107-116.
11. Botsford J.L., Harman J.G. Cyclic AMP in prokaryotes. Microbiol. Rev. 1992, 56:100-122.
12. Branda S.S., Vik A., Friedman L., Kolter R. Biofilms: the matrix revisited. Trends Microbiol. 2005, 13:20-26.
13. Brombacher E., Dorel C., Zehnder A.J.B., Landini P. The curli biosynthesis regulator CsgD co-ordinates the expression of both positive and negative determinants for biofilm formation in Escherichia coli. Microbiology 2003, 149:2847-2857.
14. Brombacher E., Baratto A., Dorel C., Landini P. Gene expression regulation by the curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J. Bacteriol. 2006, 188:2027-2037.
15. Brown P.K., Dozois C.M., Nickerson C.A., Zuppardo A., Terlonge J., Curtiss R. MlrA, a novel regulator of curli (Agf) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar typhimurium. Mol. Microbiol. 2001, 41:349-363.
16. Chan C., Paul R., Samoray D., Amiot N., Giese B., Jenal U., Schirmer T. Structural basis of activity and allosteric control of diguanylate cyclase. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:17084-17089.
17. Chang A.L., Tuckerman J.R., Gonzalez G., Mayer R., Weinhouse H., Volman G., Amikam D., Benziman M., Gilles-Gonzalez M.-A. Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 2001, 40:3420-3426.
18. Chevance F.F.V., Hughes K.T. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 2008, 6:455-465.
19. Chin K.-H., Lee Y.-C., Tu Z.-L., Chen C.-H., Tseng Y.-S., Yang J.-M., Ryan R.P., McCarthy Y., Dow J.M., Wang A.H.-J., Chou S.-H. The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J. Mol. Biol. 2009, (December 17; Epub ahead of print).
20. Christen M., Christen B., Folcher M., Schauerte A., Jenal U. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 2005, 280:30829-30837.
21. Christen B., Christen M., Paul R., Schmid F., Folcher M., Jenoe P., Meuwly M., Jenal U. Allosteric control of cyclic di-GMP signaling. J. Biol. Chem. 2006, 281:32015-32024.
22. Dow J.M., Fouhy Y., Lucey J.F., Ryan R.P. The HD-GYP domain, cyclic di-GMP signaling, and bacterial virulence to plants. Mol. Plant Microbe Interact. 2006, 19:1378-1384.
23. Duerig A., Folcher M., Abel S., Nicollier M., Schwede T., Amiot N., Giese B., Jenal U. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 2009, 23:93-104.
24. Fang X., Gomelsky L. A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol. Microbiol. 2010, 76:1295-1305.
25. Friedman L., Kolter R. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J. Bacteriol. 2004, 186:4457-4465.
26. Galperin M.Y. Bacterial signal transduction network in a genomic perspective. Environ. Microbiol. 2004, 6:552-567.
27. Galperin M.Y. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 2005, 5:35.
28. Galperin M.Y., Nikolskaya A.N., Koonin E.V. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 2001, 203:11-21.
29. Girgis H.S., Liu Y., Ryu W.S., Tavazoie S. A comprehensive genetic characterization of bacterial motility. PLoS Genetics 2007, 3:e154.
30. Hall-Stoodley L.k., Costerton J.W., Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2004, 2:95-108.
31. Hasegawa K., Masuda S., Ono T.A. Light induced structural changes of a full-length protein and its BLUF domain in YcgF (Blrp), a blue-light sensing protein that uses FAD (BLUF). Biochemistry 2006, 45:3785-3793.
32. Hengge R. Principles of cyclic-di-GMP signaling. Nat. Rev. Microbiol. 2009, 7:263-273.
33. Hengge R. Cyclic-di-GMP reaches out into the bacterial RNA world. Sci. Signal. 2010, 3:pe44.
34. Hengge R. Role of c-di-GMP in the regulatory networks of Escherichia coli. The Second Messenger Cyclic-di-GMP 2010, 230-252. ASM Press, Washington, DC. A.J. Wolfe, K.L. Visick (Eds.).
35. Hengge R. The general stress response in Gram-negative bacteria. Bacterial Stress Responses 2011, 251-289. ASM Press, Washington, DC. G. Storz, R. Hengge (Eds.).
36. S subunit of RNA polymerase in Escherichia coli. Microbiol. Mol. Biol. Rev. 2002, 66:373-395.
37. Hickman J.W., Harwood C.S. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 2008, 69:376-389.
38. Hickman J.W., Tifrea D.F., Harwood C.S. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:14422-14427.
39. Ho Y.S., Burden L.M., Hurley J.H. Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor. EMBO J. 2000, 19:5288-5299.
40. Jenal U. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria?. Curr. Opin. Microbiol. 2004, 7:185-191.
41. Jenal U., Malone J. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 2006, 40:385-407.
42. Jonas K., Edwards A.N., Simm R., Romeo T., Römling U., Melefors O. The RNA binding protein CsrA controls c-di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol. Microbiol. 2008, 70:236-257.
43. Kaper J.B., Nataro J.P., Mobley H.L.T. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2:123-140.
44. Kulasakara H., Lee E., Brencic A., Liberati N., Urbach J., Miyata S., Lee D.G., Neely A.N., Hyodo M., Hayakawa Y., Ausubel F.M., Lory S. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterase reveals a role for bis-(3ó-5ó)-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2839-2844.
45. Kumar M., Chatterji D. Cyclic-di-GMP: a second messenger required for long-term survival, but not for biofilm formation, in Mycobacterium smegmatis. Microbiology 2008, 154:2942-2955.
46. Leduc J.L., Roberts G. Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J. Bacteriol. 2009, 191:7121-7122.
47. Lee V.T., Matewish J.M., Kessler J.L., Hyodo M., Hayakawa Y., Lory S. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol. Microbiol. 2007, 65:1474-1484.
48. Lee E.R., Baker J.L., Weinberg Z., Sudarsan N., Breaker R.R. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 2010, 845-848.
49. Malone J., Williams R., Christen M., Jenal U., Spiers A.J., Rainey P.B. The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology 2007, 153:980-994.
50. Merighi M., Lee V.T., Hyodo M., Hayakawa Y., Lory S. The second messenger bis-(3ó-5ó)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 2007, 65:876-895.
51. Newell P.D., Monds R.D., O'Toole G.A. LapD is a bis-(3ó,5ó)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3461-3466.
52. Paul R., Weiser S., Amiot N., Chan C., Schirmer T., Giese B., Jenal U. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 2004, 18:715-727.
53. Paul K., Nieto V., Carlquist W.C., Blair D.F., Harshey R.M. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a " backstop brake" mechanism. Mol. Cell 2010, 38:128-139.
54. Pesavento C., Hengge R. Bacterial nucleotide-based second messengers. Curr. Opin. Microbiol. 2009, 12:170-176.
55. Pesavento, C., Hengge, R., 2012. The global repressor FliZ antagonizes gene expression by sigmaS-containing RNA polymerase due to overlapping DNA binding specificity. Nucl. Acids Res., in revision.
56. Pesavento C., Becker G., Sommerfeldt N., Possling A., Tschowri N., Mehlis A., Hengge R. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev. 2008, 22:2434-2446.
57. Prigent-Combaret C., Brombacher E., Vidal O., Ambert A., Lejeune P., Landini P., Dorel C. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 2001, 2001:7213-7223.
58. Rao F., Yang Y., Qi Y., Liang Z.X. Catalytic mechanism of c-di-GMP specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J. Bacteriol. 2008, 190:3622-3631.
59. Römling U., Amikam D. Cyclic di-GMP as a second messenger. Curr. Opin. Microbiol. 2006, 9:218-228.
60. Römling U., Sierralta W.D., Eriksson K., Normark S. Multicellular and aggregative behaviour of Salmonella typhimurum strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 1998, 28:249-264.
61. Römling U., Rohde M., Olsén A., Normark S., Reinköster J. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 2000, 36:10-23.
62. Ross P., Weinhouse H., Aloni Y., Michaeli D., Weinberger-Ohana P., Mayer R., Braun S., de Vroom E., van der Marel G.A., van Boom J.H., Benziman M. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylate. Nature 1987, 325:279-281.
63. Ryan R.P., Fouhy Y., Lucey J.F., Crossman L.C., Spiro S., He Y.-W., Zhang L.-H., Heeb S., Williams P., Dow J.M. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6712-6717.
64. Ryan R.P., McCarthy Y., Andrade M., Farah C.S., Armitage J.P., Dow J.M. Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5989-5994.
65. Ryjenkov D.A., Tarutina M., Moskvin O.V., Gomelsky M. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 2005, 187:1792-1798.
66. Ryjenkov D.A., Simm R., Römling U., Gomelsky M. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ protein YcgR controls motility in enterobacteria. J. Biol. Chem. 2006, 281:30310-30314.
67. Schirmer T., Jenal U. Structural and mechanistic determinants of c-di-GMP signalling. Nat. Rev. Microbiol. 2009, 7:724-735.
68. Schmidt A.J., Ryjenkov D.A., Gomelsky M. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 2005, 187:4774-4781.
69. Seshasayee A.S., Fraser G.M., Luscombe N.M. Comparative genomics of cyclic-di-GMP signalling in bacteria: post-translational regulation and catalytic activity. Nucleic Acids Res. 2010, 38:5970-5981.
70. Simm R., Morr M., Kader A., Nimtz M., Römling U. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 2004, 53:1123-1134.
71. Simm R., Lusch A., Kader A., Andersson M., Römling U. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar typhimurium. J. Bacteriol. 2007, 189:3613-3623.
72. Sommerfeldt N., Possling A., Becker G., Pesavento C., Tschowri N., Hengge R. Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 2009, 155:1318-1331.
73. Sudarsan N., Lee E.R., Weinberg Z., Moy R.H., Kim J.N., Link K.H., Breaker R.R. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 2008, 321:411-413.
74. Suzuki K., Babitzke P., Kushner S.R., Romeo T. Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev. 2006, 20:2605-2617.
75. Tal R., Wong H.C., Calhoon R., Gelfand D., Fear A.L., Volman G., Mayer R., Ross P., Amikam D., Weinhouse H., Cohen A., Sapir S., Ohana P., Benziman M. Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J. Bacteriol. 1998, 180:4416-4425.
76. Tamayo R., Tischler A.D., Camilli A. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 2005, 280:33324-33330.
77. Tischler A.D., Camilli A. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 2005, 73:5873-5882.
78. Tschowri N., Busse S., Hengge R. The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue light response of E. coli. Genes Dev. 2009, 23:522-534.
79. Tuckerman J.R., Gonzalez G., Gilles-Gonzalez M.-A. Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J. Mol. Biol. 2011, 407:633-639.
80. Wada T., Morizane T., Abo T., Tominaga A., Inoue-Tanaka K., Kutsukake K. EAL domain protein YdiV acts as an anti-FlhD4C2 factor responsible for nutritional control of the flagellar regulon in Salmonella enterica Serovar Typhimurium. J. Bacteriol. 2011, 193:1600-1611.
81. Wan X., Tuckerman J.R., Saito J.A., Freitas T.A.K., Newhouse J.S., Denery J.R., Galperin M.Y., Gonzalez G., Gilles-Gonzalez M.-A., Alam M. Globins synthesize the second messenger bis-(3ó-5ó)-cyclic diguanosine monophosphate in bacteria. J. Mol. Biol. 2009, 388:262-270.
82. Wang X., Preston J.F.R., Romeo T. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J. Bacteriol. 2004, 186:2724-2734.
83. S network of Escherichia coli. Mol. Microbiol. 2006, 62:1014-1034.
84. Wolfe A.J., Visick K.L. The Second Messenger Cyclic-di-GMP 2010, ASM Press, Washington, DC.
85. Zhao K., Liu M., Burgess R.R. Adaptation in bacterial flagellar and motility systems: from regulon members to " foraging" -like behavior in E. coli. Nucleic Acids Res. 2007, 35:4441-4452.